Vibrio Fluvialis: an Emerging Human Pathogen

REVIEW ARTICLE published: 07 March 2014 doi: 10.3389/fmicb.2014.00091 Vibrio ﬂuvialis: an emerging human pathogen

Thandavarayan Ramamurthy 1*, Goutam Chowdhury 1, Gururaja P.Pazhani 1 and Sumio Shinoda 2

1 National Institute of Cholera and Enteric Diseases, Kolkata, India 2 National Institute of Cholera and Enteric Diseases, Collaborative Research Center of Okayama University for Infectious Diseases in India, Kolkata, India

Edited by: Vibrio fluvialis is a pathogen commonly found in coastal environs. Considering recent Rita R. Colwell, University of increase in numbers of diarrheal outbreaks and sporadic extraintestinal cases, V.fluvialis has Maryland, USA been considered as an emerging pathogen. Though this pathogen can be easily isolated Reviewed by: by existing culture methods, its identification is still a challenging problem due to close Carlos R. Osorio, University of Santiago de Compostela, Spain phenotypic resemblance either with Vibrio cholerae or Aeromonas spp. However, using Brian Austin, University of Stirling, UK molecular tools, it is easy to identify V. fluvialis from clinical and different environmental *Correspondence: samples. Many putative virulence factors have been reported, but its mechanisms of Thandavarayan Ramamurthy, National pathogenesis and survival fitness in the environment are yet to be explored. This chapter Institute of Cholera and Enteric covers some of the major discoveries that have been made to understand the importance Diseases, P-33, CIT Road, Scheme-XM, Beliaghata, of V. fluvialis. Kolkata-700010, India Keywords:V. fluvialis, diarrhea, virulence factors, antimicrobial resistance, molecular typing e-mail: [email protected]

INTRODUCTION importance of V. fluvialis (Chowdhury et al., 2012; Liang et al., Vibrio fluvialis is a halophilic Gram-negative bacterium, which 2013). has a curved cell morphology and polar flagella for motility. The important biochemical features of this organism include IDENTIFICATION AND TAXONOMY conversion of nitrate to nitrite, do not cleave L-lysine or Thiosulfate-citrate-bile salts-sucrose agar (TCBS) has been con- ornithine, activate arginine dihydrolase, produce indole but ventionally used as a selective medium for the isolation of clinically not acetoin, ferment sucrose, D-mannitol, L-arabinose, maltose, important vibrios. The colony morphology of V. fluvialis in this trehalose, D-galactose, and D-galacturonate. Most of the vib- medium remains indistinguishable from V. cholerae, i.e., it grows rios, including V. fluvialis occur widely in the aquatic milieu, as sucrose fermenting yellow color colonies after direct plating of mostly in the seas, estuaries and brackish waters. Even though clinical specimens or after enrichment in alkaline peptone water more than 100 spices have been reported in the Genus Vib- (pH 8.0). After preliminary screening in the TCBS, a battery rio (http://www.bacterio.net/uw/vibrio.html), about 13 of them of biochemical testes is essential for the species-specific identi- have been reported to cause several human diseases. Among fication of V. fluvialis. Minimal biochemical tests such as lysine the pathogenic vibrios, V. alginolyticus, V. cholerae, V. costicola, decarboxylase, ornithine decarboxylase, arginine dihydrolase, and V. mimicus, V. cincinnatiensis, V. hollisae, V. furnissii, V. para- L-arabinose are mandatory for the identification of V. fluvialis. haemolyticus, V. vulnificus, V. carchariae (a junior synonym of Without these minimal tests, the identification is incomplete and V. harveyi) and V. metschnikovii are clinically important as they the isolate will be improperly classified as V. cholerae or Aeromonas cause different types of vibriosis. One of the Vibrio spp., V. spp. In most resource-poor countries, these tests are not method- damselae has now been renamed as “Photobacterium damselae ically performed, which may lead to labeling of V. fluvialis as subsp. damselae.” The toxigenic V. cholerae, V. parahaemolyti- V. cholerae. Considering such situation, there is a high possibil- cus and V. vulnificus are associated with well-known cholera ity that the V. fluvialis could be reported as V. cholerae non-O1, and diarrhea and extraintestinal infections, respectively. Preva- non-O139 or non-agglutinable vibrios (NAGs). It is worth to lence of V. cholerae in developing countries is mostly related mention here that V. cholerae O1 and O139 serogroups can to the breakdown of sanitary conditions and/or due to scarcity be easily confirmed by slide agglutination with corresponding of drinking water. On the other hand, infections caused by antiserum. V. parahaemolyticus and other vibrios denote contamination For the identification of V. fluvialis and other vibrios, rapid of seafood in many countries, irrespective of their economic identification kits must be used with caution as they need conditions. additional tests for the final confirmation. While testing the com- V. fluvialis is one of the emerging foodborne pathogens all over mercially available identification kits, V.fluvialis remain as a major the world. The distribution of virulence factors and molecular epi- challenge with API 20E and Vitek GNI+ systems (Israil et al., 2003; demiological features of this pathogen remain mostly unknown. O’Hara et al., 2003). Biochemically, V. furnissii expresses fibrin Among the foodborne infections in the United States, there and mucin hydrolysis but no phosphate or esculin hydrolysis, for has been a considerable increase (43%) in the Vibrio-mediated which V. fluvialis varied. V. fluvialis, V. furnissii, and V. mimicus are infections till 2012 compared with the rates reported during distinctive from V. cholerae, as the later exhibit strong mannose- 2006–2008 (Centers for Disease Control and Prevention (CDC), sensitive hemagglutination. These test results may have a strong 2013). Several recent publications indicate the epidemiological influence in the confirmation of strains.

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Molecular tools such as PCR are useful in the identification for the identification of V. fluvialis and with a set of phages, of many uncommon vibrios and most of these assays are com- the diagnostic probability of human isolates was more than parable to the conventional identification methods. The sequence 84%. At least in one study, the importance of phage-typing of amplified 16S–23S intergenic spacers (IGSs) has demonstrated of V. fluvialis has been demonstrated using six specific bac- 37 ribosomal RNA (rrn) operons representing seven different IGS teriophages with 73% typability (Suthienkul, 1993). However, types in different Vibrio spp. with IGS(0), IGS(IA), and IGS(Glu) availability of these bacteriophages makes this assay technique less as major ones. The sequence difference in these IGS types was popular. used to design species-specific primers for PCR for V. fluvialis and other vibrios (Lee et al., 2002). In some of the reports, a uni- PHENOTYPIC AND GENETIC CHARACTERISTICS OF versal primer PCR that covers conserved regions of bacterial 16S V. fluvialis rRNA genes followed by denaturing gradient gel electrophoresis Based on the somatic antigen variation, several serotypes of (DGGE) was found to be useful in the identification of V. flu- V. fluvialis have been identified. Though Shimada et al. (1999) vialis either as axenic bacteria or mixed with other pathogens identified more than 50 somatic antigens, the serological based (Ji et al., 2004). typing of V. fluvialis remains non-customary. V. fluvialis strains Initially, V. furnissii was taxonomically assigned with V. fluvialis belonging to serogroup O19 possessed the C (Inaba) antigen of and named as aerogenic biogroup of V. fluvialis.BasedonDNA V. cholerae O1, but not the B (Ogawa) or A (common) anti- relatedness and several biochemical tests, V. furnissii has been sep- gens (Shimada et al., 1987; Kondo et al., 2000). In the crossed arated as a new species (Lee et al., 1981; Brenner et al., 1983). In the immuno-electrophoresis, antibodies against the oral cholera vac- phylogenetic analysis with several housekeeping genes, V. furnissii cines containing killed whole cells (WC) of V. cholerae O1 Inaba and V. fluvialis have been linked as close species. The nucleotide El Tor reacted with a few strains of V. fluvialis (Ciznãr et al., 1989). comparison of 16S-rRNA, recA, and toxR sequences showed that Presence of shared WC antigens indicates that the oral cholera V. furnissii and V. fluvialis had 100% similarity. The gene toxR of V. vaccine could stimulate immunity effectively against other vib- fluvialis had 84% similarity with V.harveyi (Franco and Hedreyda, rios also. It is known that the antigenic nature of flagella of 2006). With the gyrB, V. cholerae, V. mimicus, V. furnissii, and V. vibrios is highly homologous. Tassin et al. (1983) and Shinoda fluvialis shared 93% sequence similarity. et al. (1984) demonstrated independently that anti-L-flagella anti- Toxigenic vibrios have a homolog of the toxRS operon, which sera of V. fluvialis did not agglutinate other Vibrio species in the regulates the virulence expression. The gene toxR encodes a tran- H-agglutination tests. Further studies placed V.fluvialis and V.fur- scriptional activation domain (TAD), a transmembrane domain nissii in the same lateral flagellar serogroup-HL8 (Shinoda et al., (TMD), and a periplasmic domain (PD). Among the vibrios, 1992). However, in practice, serotyping based on H-flagella is also there is essentially no homology within the region between TAD not in use. and TMD. Hence, this region has been used in designing of A chemotaxonomic study based on sugar composition of primers for the species-specific identification of many vibrios. the polysaccharide portion of their lipopolysaccharide (LPS) has Chakraborty et al. (2006) described a species-specific identifica- divided 35 O-antigen groups of V. fluvialis into 21 chemotypes tion of V.fluvialis by PCR targeted to the conserved transcriptional (Iguchi et al., 1993). This seems to be a unique finding since the activation and variable membrane tether regions of the toxR D-glycero-D-manno-heptose, and two kinds of uronic acids, i.e., gene. The functional virulence genes encoding hemolysin (vfh), galacturonic and glucuronic acids are rare in Gram-negative bac- heme-utilization (hupO), and central regulation (vfpA)havebeen teria. In addition, 2-keto-3-deoxyoctonate, which is a typical sugar used as targets in an multiplex PCR for the identification of component of Gram-negative bacterial LPS was not detectable in V. cholerae, V. parahaemolyticus, and V. fluvialis, respectively any of the chemotypes. (Vinothkumar et al., 2013). For the detection of clinical vib- Of all the molecular typing methods, the pulsed-field gel elec- rios in seafood samples, a multiplex primer-extension reaction trophoresis (PFGE) has proven to be highly useful in tying the (PER) assay targeting the rpoA gene has also been reported bacterial isolates. Unlike V. cholerae O1 and pandemic V. para- (Dalmasso et al., 2009). haemolyticus, the isolates of V. fluvialis from acute diarrheal Pyrolysis-mass spectrometry with metastable atom bombard- patients exhibited large genetic diversity (Chowdhury et al., 2012, ment and pattern recognition seemed to be suitable for the 2013). identification of V. fluvialis and other vibrios (Wilkes et al., 2005). The mass spectra have been generated via an alternative ion- PREVALENCE OF V. fluvialis IN THE AQUATIC REALM ization method, metastable atom bombardment followed by Even though the presence of vibrios is mostly documented from component-discriminant analysis. Since the outer membrane pro- coastal environs, the domination of a particular species depends on tein K (OmpK) of V. fluvialis, V. alginolyticus, V. mimicus, V. many physico-chemical and biological factors. In warmer regions parahaemolyticus, and V. vulnificus is highly similar, the antibod- like Florida, USA, V. fluvialis was predominantly detected in sed- ies against these proteins have been proposed in the diagnosis (Li iments during winter months (Williams and Larock, 1985). Due et al., 2010). The whole cell protein profile using SDS-PAGE was to rise in seawater temperature, the identification rate of V. flu- also considered in the identification of clinically important vibrios vialis has increased considerably (29%) in several niches at the including V. fluvialis (Lee et al., 2012). Toulon harbor, France (Martin and Bonnefont, 1990). However, Since simple phenotypic diagnostic tests are not available, in Chesapeake Bay, V. fluvialis infections are always less during Chen et al. (1995) used species-specific bacteriophages as a tool winter months, indirectly reflecting its minimal occurrence in

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this season (Hoge et al., 1989). V. fluvialis along with V. vulnifi- In the marine environment, V. fluvialis plays a major role in cus and V. cholerae non-O1 unusually existed in the Seto Inland the production of hydrogen from starch acquired from the algal Sea of Japan, which is a eutrophic zone with riverine influence mass in the presence of Rhodobium marinum. In co-culture experi- (Venkateswaran et al., 1989a). In South East Queensland, Aus- ments, V.fluvialis degrade starch leading to the formation of acetic tralia, next to V. cholerae (10.2%), V. fluvialis (8.2%) has been acid and ethanol, which are subsequently utilized for hydrogen isolated more frequently from river waters, sediments, and plants production by R. marinum (Ike et al., 1999). (Myatt and Davis, 1989). Due to high load of pollution in the upstream of the river SPORADIC CASES AND OUTBREAKS OF DIARRHEA DUE TO Ganges, presence of V. fluvialis (0.74%) with other potential V. fluvialis pathogens have been detected in several points of Varanasi, India Early reports from the US indicated involvement of V. fluvi- (De et al., 1993). V. fluvialis has also been isolated from natu- alis with gastroenteritis among infants (Hickman-Brenner et al., ral waters in Myanmar (Oo et al., 1993) and in a wide range of 1984; Bellet et al., 1989; Kolb et al., 1997). Since 1979, V. flu- coastal environments of Japan (Uchiyama, 2000). Compared to vialis was isolated as one of the important pathogens in Tenri other vibrios, the recovery of V. fluvialis has been high (41.4%) Hospital, Japan (Aihara et al., 1991). Prevalence of V. fluvialis from suburban community effluents in South Africa. However, among children with diarrhea was very less during 1988 (0.6%) their occurrence was not associated with any season or plankton in Calcutta (now, Kolkata), India (Chatterjee et al., 1989). In the blooms, but positively correlated with temperature, salinity, and same region, progressive increase in the prevalence of V. fluvi- dissolved oxygen (Igbinosa et al., 2011a). alis (>2%) among hospitalized acute diarrheal patients has been In many investigations, the detection frequency of V. fluvi- reported in the following years (Chowdhury et al., 2012). During alis was very high in marine mollusks, mostly in bivalves, as 1996–1998, prevalence of V. fluvialis was 9.4% among hospital- they accumulate large number of pathogens during the process ized diarrheal patients in North Jakarta (Lesmana et al., 2002). In of filter-feeding. Findings of Kelly and Stroh (1988) from Pacific Zhejiang Province, China, V. fluvialis was identified as the sec- Northwest showed that oysters are the main source of V. flu- ond most pathogen (12%) among acute diarrheal cases but next vialis and other vibrios especially during warmer seasons. In to V. parahaemolyticus (64%; Jiang, 1991). Investigations carried Hong Kong, V. fluvialis was one of the important pathogenic vib- out after the 1998 floods in Bangladesh showed involvement of V. rios identified in coastal waters and seafood sold in the markets fluvialis in a diarrhea outbreak (Tanabe et al., 1999). However, the (Chan et al., 1986, 1989). V. fluvialis has been isolated from mus- number of cases was less compared to V. cholerae O1 and O139 sels from Senegal (Schandevyl et al., 1984), Brazil (Matté et al., infections. 1994), bivalves and mud from Costa Rica (García and Antil- Vibrio-mediated infections frequently occur in countries where lón, 1990) and cultured fishes from Denmark (Pedersen et al., the raw seafood is largely consumed. In many instances, V. fluvi- 1999), copepods from Southern Italy (Dumontet et al., 2000) alis was found to be associated with cholera-like diarrhea (Allton and cockles of Malaysia (Elhadi et al., 2004). In Turkey, next to et al., 2006). Between 1982 and 1988, 10 gastroenteritis cases V. alginolyticus (>30%), V. fluvialis was the most common Vib- of V. fluvialis have been reported in Florida due to consump- rio in blue crabs and retail fishes (>10%; Yalcinkaya et al., 2003; tion of contaminated seafood (Klontz and Desenclos, 1990). In Yücel and Balci, 2010). the Gulf coast, the majority of the Vibrio-mediated gastroenteri- Generally, fecal pollution has been monitored in aquacul- tis has been associated with intake of raw oysters and in about ture areas to forecast human pathogens in the products. In Italy, 6% of the cases V. fluvialis was the causative pathogen (Levine about 11–27% of the mollusks and shrimps contained V. fluvialis and Griffin, 1993). Foodborne outbreaks were reported in several without any association between presence of this pathogen and communities implicating V. fluvialis alone or with either V. para- conventional fecal pollution indicators (Ripabelli et al., 2004). The haemolyticus/Salmonella spp. (Tokoro et al., 1984; Chowdhury micro fauna and flora occasionally support the occurrence human et al., 2013). pathogens. V. fluvialis (36.5%) was significantly associated with Foodborne diarrheal outbreaks caused by V. fluvialis have been plankton in the effluents of a rural wastewater treatment facility in reported during 1981 in Maharashtra (Thekdi et al., 1990) and the Eastern Cape Province of South Africa (Igbinosa et al., 2009). 2012 in Kolkata (Chowdhury et al., 2013). In Brazil, and USSR, In the Atlantic coast of France, Deter et al. (2010) showed that the first report on the association of V. fluvialis with diarrhea was chlorophyll-A had a significant influence on pathogenic vibrios reported during 1990 and 1991, respectively (Magalhães et al., including V. fluvialis in mussels. 1990; Libinzon et al., 1991). Though the incidence of cholera There are few reports about identification of V. fluvialis from among high socioeconomic population in Brazil was very low wound infections that took place in recreational areas. Since (0.07%), but the other vibrios including V. fluvialis comparatively V. fluvialis has been cultured from the teeth of a great white prevailed more (1.2%; Magalhães et al., 1993). In Volga delta, Rus- shark (Carcharodon carcharias), there may be an association sia, acute enteric infections caused by V. fluvialis reaches about of this pathogen with wound infections caused by sharks in 30% during the summer months, mainly due to consumption of humans (Buck et al., 1984). Fibropapillomatosis (FP) is a muti- water than sea/fresh water fishes (Bo˘iko, 2000). Among travelers lating disease among turtles that cause tumors on the skin and with diarrheal symptoms, the incidence of V. fluvialis seemstobe other internal organs. In a study conducted by Aguirre et al. low compared to other enteric pathogens. Early studies conducted (1994) showed the presence of V. fluvialis (47%) in green turtles with US Peace Corps volunteers in Thailand identified V. fluvialis with FP. in about 3% of the cases (Taylor et al., 1985).

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OTHER INFECTIONS culture supernatant retained hemolytic and phospholipase A2 Vibrio fluvialis causes a variety of infections in immune- activities and were coeluted in the gel filtration (Wall et al., 1984). competent/HIV patients, including bacteremia, biliary tract infec- The purified extracellular hemolysin produced by V. fluvialis tion and acute diarrhea (Albert et al., 1991; Usó et al., 2010; Liu showed virulence features including lyses of erythrocytes of differ- et al., 2011). The other rarely reported infections caused by this ent animal origin and activation of fluid accumulation in suckling pathogen include suppurative cholangitis (Yoshiiet al.,1987), peri- mice (Han et al., 2002; Kothary et al., 2003). tonitis (Lee et al., 2008), acute otitis (Cabrera et al., 2005; Chen The transmembrane regulatory protein (ToxR) is essential for et al., 2012) and endophthalmitis (Penland et al., 2000). Large the expression of virulence factors in pathogenic vibrios. Similar numbers of (29%) endophthalmitis patients were reported to have to V. cholerae, the ToxR plays a major role in bile resistance of V. mixed infection with V. fluvialis (Hassan et al., 1992). A report fluvialis, which is an initial phase in the progression of vibrios as from Cuba showed that V. fluvialis was one of the predominantly potential intestinal pathogens (Provenzano et al., 2000). Adapt- identified pathogens from different extraintestinal samples (Cabr- ability of vibrios to the intestinal environment, especially the bile era et al., 2007). Cases of bacteremia with diarrhea (Lai et al., salts favors colonization and expression of virulence factors. After 2006) hemorrhagic cellulitis and cerebritis (Huang and Hsu,2005), initial adaptation to the bile salts under in vitro conditions, the peritonitis (Ratnaraja et al., 2005) have also been reported. V. fluvialis exhibited swarming mobility, biofilm formation and adherence (Di Pietro et al., 2004). In the animal models, V. fluvi- QUORUM SENSING alis and the cholera toxin (CT) produced by V. cholerae O1 strains Quorum sensing (QS) is a process in which bacterial cells in a pop- confirmed skin permeability factor (SPF). However, the antibod- ulation are able to crosstalk with one another, thereby supporting ies against CT did not neutralize the SPF of V. fluvialis (Rodrigues them as a unit to synchronize gene regulation and consequent phe- et al., 1993; Ahsan et al., 1988). notypic changes. The importance of QS in pathogenic V. cholerae The exocellular metalloprotease produced by V. fluvialis (VFP) has been well established. Wang et al. (2013) have shown that QS was found to be similar to the one produced by V.vulnificus, which in V. fluvialis regulates two potential virulence factors, includ- has also been used for the hemagglutination activity (Miyoshi ing an extracellular protease and hemolysin. In addition, QS also et al., 2002). In addition, the amino acid sequence of VFP was regulates in vitro cytotoxic activity against epithelial cell lines. found to be a member of the thermolysin family. It is interesting to note that most of the V. fluvialis isolated from the diarrheal VIRULENCE FACTORS patients harbored genes encoding hemolysin and metalloprotease The clinical as well as environmental V. fluvialis strains express (Chowdhury et al., 2012). many putative virulence factors. The common virulence factor in V. fluvialis reported in several investigations is the expression of SURVIVAL hemolysin that can be easily identified in sheep-blood agar plates. Vibrio fluvialis has the capacity to survive in the seawater micro- In majority of the toxin detection assays, eukaryotic cell lines are cosm for more than 15 days at ambient temperature regardless of being used in vitro. In cell-free extracts, V. fluvialis has expressed carbonated substrate uptake (Munro et al., 1994). In microcosms, Chinese hamster ovary (CHO) cell elongation factor, CHO cell- V. fluvialis has been shown culturally viable for a year without killing factors, cytolysins against erythrocytes and proteases active losing its virulence and in sediments this organism was recovered against azocasein (Lockwood et al., 1982). Various putative viru- from viable but non-culturable stage, even after 6 years (Amel lence factors of V. fluvialis are presented in Table 1. However, the et al., 2008). ability to produce these factors is not uniform in all the isolates (Liang et al., 2013). ANTIMICROBIAL RESISTANCE Purification of cytotoxin produced by V. fluvialis showed that Compared to other clinical vibrios, antimicrobial resistance the protein was heat-labile, and deactivated by proteases. The (AMR) is largely reported in V. fluvialis. In Mediterranean fish farms, many of the vibrios including V. fluvialis were resistant to ampicillin, carbenicillin, kanamycin, cefalotin, and Table 1 | Different putative virulence factors described in V. fluvialis. sulfadiazine-trimethoprim (Laganà et al., 2011). In South Africa, treated effluent system was found to be the reservoir for V. Factor Reference fluvialis strains, which are resistant to ampicillin, penicillin-G, streptomycin, sulfamethoxazole, trimethoprim, chlorampheni- Cytolysin Lockwood et al. (1982) col, erythromycin, ciprofloxacin, and polymyxin B (Igbinosa Heat-labile cytotoxin Wall et al. (1984) et al., 2011b). In China, majority of the V. fluvialis strains Cytotonic Venkateswaran et al. (1989b) were resistant for β-lactams, azithromycin, and sulfamethoxazole Hemolysin Wong et al. (1992) (Liang et al., 2013). Mucinase Janda (1986) Several mobile genetic elements carrying AMR have been found in V. fluvialis. The integrative and conjugative element (ICE) Mannose sensitive Rahman et al. (1992) is a conjugative transposon commonly detected in V. cholerae, hemaagglutination which carries resistance genes for sulfamethoxazole-trimethoprim Cell adherence Carvalho et al. (1994), Scoglio et al. (2001) (SXT), chloramphenicol and streptomycin (Srinivasan et al., 2006; Cell vaculation Chakraborty et al. (2005) Taviani et al., 2008). This SXT element has also been reported

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in V. fluvialis that has integrase gene similar to that of V. cholerae Allton, D. R., Forgione, M. A. Jr., and Gros, S. P. (2006). Cholera-like (Ahmed et al., 2005). The aminoglycoside acetyltransferase encod- presentation in Vibrio fluvialis enteritis. South Med. J. 99, 765–767. doi: ing gene aac(3)-Id was identified in class 1 integron from a clinical 10.1097/01.smj.0000223657.22296.e6 Amel, B. K., Amine, B., and Amina, B. (2008). Survival of Vibrio fluvialis V. fluvialis strains (Ahmed et al., 2004). in seawater under starvation conditions. Microbiol. Res. 163, 323–328. doi: Transfer of large plasmids carryingAMR genes is rarely detected 10.1016/j.micres.2006.06.006 in V. fluvialis (Rajpara et al., 2009). Efflux systems responsible for Bellet, J., Klein, B., Altieri, M., and Ochsenschlager, D. (1989). Vibrio fluvialis, nalidixic acid and ciprofloxacin resistance have been reported in an unusual pediatric enteric pathogen. Pediatr. Emerg. Care 5, 27–28. doi: several clinical V. fluvialis strains (Srinivasan et al., 2006). Two 10.1097/00006565-198903000-00008 Boˇiko, A. V. (2000). The etiological structure of acute intestinal infections caused putative multi antimicrobial extrusion (MATE) protein family by noncholera vibrios in the Volga delta. Zh. Mikrobiol. Epidemiol. Immunobiol. efflux pumps viz., H- and D-type were found to be responsible 1, 15–17. [In Russian]. for fluoroquinolones resistance in V. fluvialis. The sequences of Brenner, D. J., Hickman-Brenner, F. W., Lee, J. V., Steigerwalt, A. G., Fanning, G. R., these MATE encoding genes were found to be ∼99% identical to Hollis, D. G., et al. (1983). Vibrio furnissii (formerly aerogenic biogroup of Vibrio V. cholerae (Mohanty et al., 2012). In addition, many V. fluvialis fluvialis), a new species isolated from human feces and the environment. J. Clin. Microbiol. 18, 816–824. strains had mutation (serine to isoleucine) at position 83 of the Buck, J. 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P., Morier, L., Ramírez, A. M. M., Fernández, In addition, these strains carried a transferrable 150-kb plas- A. A., Castro, E. G., et al. (2005). Severe otitis due to Vibrio fluvialis in a mid that harbored the quinolone resistance qnrA1 in a complex patient with AIDs: first report in the world. Rev. Cubana Med. Trop. 57, 154–155. sul1-type integron, the ciprofloxacin-modifying enzyme-encoding Carvalho, I. T., Magalhães, V., Leal, N. C., Melo, V.,and Magalhães, M. (1994). Vibrio gene aac(6 )-Ib-cr and genes encoding for extended-spectrum fluvialis attaches to but does not enter HeLa cell monolayers. Mem. Inst. Oswaldo β-lactamases such as blaSHV and blaCTX−M−3. Cruz 89, 221–223. doi: 10.1590/S0074-02761994000200019 Centers for Disease Control and Prevention (CDC). (2013). Incidence, and trends CONCLUSION of infection with pathogens transmitted commonly through food – foodborne Though the pathogen V. fluvialis has known for quite some time, diseases active surveillance network, 10 U.S. sites, 1996–2012. MMWR Morb. Mortal Wkly. Rep. 62, 283–287. its clinical importance is realized now, as the prevalence of diarrhea Chakraborty, R., Chakraborty, S., De, K., Sinha, S., Mukhopadhyay, A. K., Khanam, cases is reportedly increasing. In depth studies on the pathogenesis J., et al. (2005). Cytotoxic and cell vacuolating activity of Vibrio fluvialis isolated of V. fluvialis has to be established as there are many descriptions from paediatric patients with diarrhoea. J. Med. Microbiol. 54(Pt 8), 707–716. about the putative virulence factor. doi: 10.1099/jmm.0.45820-0 Chakraborty, R., Sinha, S., Mukhopadhyay, A. K., Asakura, M., Yamasaki, S., ACKNOWLEDGMENTS Bhattacharya, S. K., et al. (2006). 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Williams, L. A., and Larock, P. A. (1985). Temporal occurrence of Vibrio species Conflict of Interest Statement: The authors declare that the research was conducted and Aeromonas hydrophila in estuarine sediments. Appl. Environ. Microbiol. 50, in the absence of any commercial or financial relationships that could be construed 1490–1495. as a potential conflict of interest. Wong, H. C., Ting, S. H., and Shieh, W. R. (1992). Incidence of toxigenic vibrios in foods available in Taiwan. J. Appl. Bacteriol. 73, 197–202. doi: 10.1111/j.1365- Received: 17 December 2013; accepted: 19 February 2014; published online: 07 March 2672.1992.tb02978.x 2014. Yalcinkaya, F., Ergin, C., Agalar, C., Kaya, S., and Aksoylar, M. Y. (2003). Citation: Ramamurthy T, Chowdhury G, Pazhani GP and Shinoda S (2014) The presence and antimicrobial susceptibilities of human-pathogen Vibrio Vibrio fluvialis: an emerging human pathogen. Front. Microbiol. 5:91. doi: spp. isolated from blue crab (Callinectes sapidus) in Belek tourism coast, 10.3389/fmicb.2014.00091 Turkey. Int. J. Environ. Health Res. 13, 95–98. doi: 10.1080/09603120210000 This article was submitted to Aquatic Microbiology, a section of the journal Frontiers 63304 in Microbiology. Yoshii,Y., Nishino, H., Satake, K., and Umeyama, K. (1987). Isolation of Vibrio fluvi- Copyright © 2014 Ramamurthy, Chowdhury, Pazhani and Shinoda. This is an open- alis, and unusual pathogen in acute suppurative cholangitis. Am. J. Gastroenterol. access article distributed under the terms of the Creative Commons Attribution License 82, 903–905. (CC BY). The use, distribution or reproduction in other forums is permitted, provided Yücel, N., and Balci, S. (2010). Prevalence of Listeria, Aeromonas, and Vib- the original author(s) or licensor are credited and that the original publication in this rio species in fish used for human consumption in Turkey. J. Food Prot. 73, journal is cited, in accordance with accepted academic practice. No use, distribution or 380–384. reproduction is permitted which does not comply with these terms.

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